Animal species not investing in parental care can nevertheless influence the success of their progeny by actively selecting sites that are most favourable for their growth and survival. Primarily through the study of phytophagous insects, it has become clear that oviposition behaviour, and choice of oviposition sites in particular, can increase the performance and survival of insect progeny. Such oviposition behaviour is largely driven by variation in the environment. In this study, we examined oviposition choice and larval survival of the senita moth (Upiga virescens), which is an obligately pollinating granivore of a single host plant, the senita cactus (Lophocereus schottii). Although senita moths oviposit only on open flowers of senita cacti, eggs are laid among four relatively discrete sites on flowers: between or underneath petals, on the outward-facing side of petals, on anthers and within the corolla tube. In a population of senita cacti in southern Arizona, we quantified the distribution of eggs among flowers and plants, the distribution of eggs among oviposition sites, and larval (egg-to-pupa) survival among oviposition sites. Eggs were evenly distributed among flowers, but plants with more flowers had greater numbers of eggs than plants with few flowers. On the other hand, eggs were unevenly distributed among oviposition sites within flowers. Eggs were most frequently laid on petals, and least frequently laid on anthers and corolla tubes. Inconsistent with this result, larval survival was greater for anthers and corolla tubes than for petals. However, taking into account differences in surface area among oviposition sites, anthers and corolla tubes received disproportionately greater numbers of eggs than expected by chance, while petals received slightly fewer eggs than expected given surface area. This result is consistent with larval survival being greater for anthers and corolla tubes. We discuss potential ecological and evolutionary reasons for why selection has apparently favoured an even distribution of eggs among flowers, but has not more strongly favoured ovipositing into corolla tubes and anthers where progeny survival is greatest.

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